P2X receptors as cell-surface ATP sensors in health and disease

Nature

Volumn 442, Issue 7102, 2006, Pages 527-532

  Khakh, Baljit S ^a,b   Alan North, R ^c  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINETRIPHOSPHATE; BIOLOGICAL MEMBRANES; CELL CULTURE; DISEASES; MOLECULAR STRUCTURE; NEUROLOGY; PROTEINS;

ATP SENSORS; AUTONOMIC NERVOUS SYSTEM; MEMBRANE ION CHANNELS; P2X RECEPTORS;

BIOSENSORS;

ADENOSINE TRIPHOSPHATE; PURINE P2X RECEPTOR;

HEALTH CARE; NERVOUS SYSTEM; PROTEIN;

AUTOCRINE EFFECT; AUTONOMIC NERVOUS SYSTEM; CELL MEMBRANE PERMEABILITY; CELL SURFACE; CENTRAL NERVOUS SYSTEM; CHRONIC PAIN; ELECTROPHYSIOLOGY; ENDOTHELIUM CELL; EPITHELIUM CELL; HUMAN; INFLAMMATION; NEUROPATHIC PAIN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; SENSOR; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION;

EID: 33746701380     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature04886     Document Type: Review

References (77)

1. Holton, P. The liberation of adenosine triphosphate on antidromic stimulation of sensory nerves. J. Physiol. (Lond.) 145, 494-504 (1959).
2. Burnstock, G. Purinergic nerves. Pharmacol. Rev. 24, 509-581 (1972).
3. Ralevic, V. & Burnstock, G. Receptors for purines and pyrimidines. Pharmacol. Rev. 50, 413-492 (1998).
4. Zimmermann, H. Extracellular metabolism of ATP and other nucleotides. Naunyn Schmiedebergs Arch. Pharmacol. 362, 299-309 (2000).
5. North, R. A. Molecular physiology of P2X receptors. Physiol. Rev. 82, 1013-1067 (2002).
6. Valera, S. et al. A new class of ligand-gated ion channel defined by P2X receptor for extracellular ATP. Nature 371, 516-519 (1994).
7. Brake, A. J., Wagenbach, M. J. & Julius, D. New structural motif for ligand-gated ion channels defined by an ionotropic ATP receptor. Nature 371, 519-523 (1994).
8. Nicke, A. et al. P2X1 and P2X3 receptors form stable trimers: a novel structural motif of ligand-gated ion channels. EMBO J. 17, 3016-3028 (1998).
9. 6 receptor subunits do not oligomerize. J. Biol. Chem. 280, 10759-10765 (2005).
10. Jiang, L. H. et al. Subunit arrangement in P2X receptors. J. Neurosci. 23, 8903-8910 (2003).
11. Roberts, J. A. & Evans, R. J. ATP binding at human P2X1 receptors. Contribution of aromatic and basic amino acids revealed using mutagenesis and partial agonists. J. Biol. Chem. 279, 9043-9055 (2004).
12. 2 receptors. J. Biol. Chem. 280, 25982-25993 (2005).
13. Unwin, N. Refined structure of the nicotinic acetylcholine receptor at 4 Å resolution. J. Mol. Biol. 346, 967-989 (2005).
14. Madden, D. R. The structure and function of glutamate receptor ion channels. Nature Rev. Neurosci. 3, 91-101 (2002).
15. 5 receptor. Mol. Pharmacol. 63, 1407-1416 (2003).
16. 2 purinoceptors: single channel recordings. J. Membr. Biol. 172, 215-223 (1999).
17. Egan, T. M. & Khakh, B. S. Contribution of calcium ions to P2X channel responses. J. Neurosci. 24, 3413-3420 (2004).
18. Doyle, D. A. Structural changes during ion channel gating. Trends Neurosci. 27, 298-302 (2004).
19. Miyazawa, A., Fujiyoshi, Y. & Unwin, N. Structure and gating mechanism of the acetylcholine receptor pore. Nature 424, 949-955 (2003).
20. Khakh, B. S., Bao, X., Labarca, C. & Lester, H. A. Neuronal P2X receptor-transmitter-gated cation channels change their ion selectivity in seconds. Nature Neurosci. 2, 322-330 (1999).
21. Doyle, D. A. Molecular insights into ion channel function. Mol. Membr. Biol. 21, 221-225 (2004).
22. Fisher, J. A., Girdler, G. & Khakh, B. S. Time resolved measurement of state specific P2X ion channel cytosolic gating motions. J. Neurosci. 24, 10475-10487 (2004).
23. Miyazawa, A., Fujiyoshi, Y., Stowell, M. & Unwin, N. Nicotinic acetylcholine receptor at 4.6Å resolution: transverse tunnels in the channel wall. J. Mol. Biol. 288, 765-786 (1999).
24. Chaumont, S., Jiang, L. H., Penna, A., North, R. A. & Rassendren, F. Identification of a trafficking motif involved in the stabilization and polarization of P2X receptors. J. Biol. Chem. 279, 29628-29638 (2004).
25. Royle, S. J., Bobanovic, L. K. & Murrell-Lagnado, R. D. Identification of a noncanonical tyrosine-based endocytic motif in an ionotropic receptor. J. Biol. Chem. 277, 35378-35385 (2002).
26. 2 channel permeability by the cytosolic domain. J. Gen. Physiol. 120, 119-131 (2002).
27. Denlinger, L. C. et al. Cutting edge: the nucleotide receptor P2X7 contains multiple protein- and lipid-interaction motifs including a potential binding site for bacterial lipopolysaccharide. J. Immunol. 167, 1871-1876 (2001).
28. 7 receptor signalling complex. EMBO J. 20, 6347-6358 (2001).
29. 2 subunits at excitatory synapses and modulates receptor function. J. Biol. Chem. 281, 4100-4108 (2006).
30. Rubio, M. E. & Soto, F. Distinct localisation of P2X receptors at excitatory postsynaptic specializations. J. Neurosci. 21, 641-653 (2001).
31. Edwards, F. A., Gibb, A. J. & Colquhoun, D. ATP receptor-mediated synaptic currents in the central nervous system. Nature 359, 144-147 (1992).
32. Jo, Y. H. & Role, L. W. Coordinate release of ATP and GABA at in vitro synapses of lateral hypothalamic neurons. J. Neurosci. 22, 4794-4804 (2002).
33. Jo, Y.-H. & Schlichter, R. Synaptic corelease of ATP and GABA in cultured spinal neurons. Nature Neurosci. 2, 241-245 (1999).
34. Pankratov, Y. V., Lalo, U. V. & Krishtal, O. A. Role for P2X receptors in longterm potentiation. J. Neurosci. 22, 8363-8369 (2002).
35. 1 receptors. Nature 403, 86-89 (2000).
36. 2 subunits contribute to fast synaptic excitation in myenteric neurons of the mouse small intestine. J. Physiol. (Lond.) 552, 809-821 (2003).
37. Gu, J. G. & MacDermott, A. B. Activation of ATP P2X receptors elicits glutamate release from sensory neuron synapses. Nature 389, 749-753 (1997).
38. Khakh, B. S. & Henderson, G. ATP receptor-mediated enhancement of fast excitatory neurotransmitter release in the brain. Mol. Pharmacol. 54, 372-378 (1998).
39. Nakatsuka, T. & Gu, J. G. ATP P2X receptor-mediated enhancement of glutamate release and evoked EPSCs in dorsal horn neurons of the rat spinal cord. J. Neurosci. 21, 6522-6531 (2001).
40. Khakh, B. S., Gittermann, D., Cockayne, D. A. & Jones, A. ATP modulation of excitatory synapses onto interneurons. J. Neurosci. 23, 7426-7437 (2003).
41. 2+ entry through presynaptic P2X receptors elicits postsynaptic firing in the brainstem autonomic network. J. Neurosci. 24, 3125-3135 (2004).
42. Bowser, D. N. & Khakh, B. S. ATP excites interneurons and astrocytes to increase synaptic inhibition in neuronal networks. J. Neurosci. 24, 8606-8620 (2004).
43. 1 receptors in the hippocampal slice. J. Neurosci. 24, 10835-10845 (2004).
44. Wieraszko, A., Goldsmith, G. & Seyfried, T. N. Stimulation-dependent release of adenosine triphosphate from hippocampal slices. Brain Res. 485, 244-250 (1989).
45. Gordon, G. R. et al. Norepinephrine triggers release of glial ATP to increase postsynaptic efficacy. Nature Neurosci. 8, 1078-1086 (2005).
46. Davalos, D. et al. ATP mediates rapid microglial response to local brain injury in vivo. Nature Neurosci. 8, 752-758 (2005).
47. 7 receptor inhibition improves recovery after spinal cord injury. Nature Med. 10, 821-827 (2004).
48. CO2 to cortical excitability via pH. Neuron 48, 1011-1023 (2005).
49. 4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 424, 778-783 (2003).
50. Coull, J. A. et al. BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 438, 1017-1021 (2005).
51. Bleehen, T. & Keele, C. A. Observations on the algogenic actions of adenosine compounds on the human blister base preparation. Pain 3, 367-377 (1977).
52. Hamilton, S. G., Warburton, J., Bhattacharjee, A., Ward, J. & McMahon, S. B. ATP in human skin elicits a dose-related pain response which is potentiated under conditions of hyperalgesia. Brain 123, 1238-1246 (2000).
53. Chen, C. C. et al. A P2X purinoceptor expressed by a subset of sensory neurons. Nature 377, 428-431 (1995).
54. 3 receptor subunits can account for ATP-gated currents in sensory neurons. Nature 377, 432-435 (1995).
55. Khakh, B. S., Humphrey, P. P. & Surprenant, A. Electrophysiological properties of P2X-purinoceptors in rat superior cervical, nodose and guinea-pig coeliac neurones. J. Physiol. (Lond.) 484, 385-395 (1995).
56. 3-deficient mice. Nature 407, 1011-1015 (2000).
57. 3 receptors. Nature 407, 1015-1017 (2000).
58. 3 subunit: a molecular target in pain therapeutics. Curr. Opin. Investig. Drugs 4, 833-840 (2003).
59. 2/3 receptors, reduces chronic inflammatory and neuropathic pain in the rat. Proc. Natl Acad. Sci. USA 99, 17179-17184 (2002).
60. Kirkup, A. J., Booth, C. E., Chessell, I. P., Humphrey, P. P. & Grundy, D. Excitatory effect of P2X receptor activation on mesenteric afferent nerves in the anaesthetised rat. J. Physiol. (Lond.) 520, 551-563 (1999).
61. Galligan, J. J. Enteric P2X receptors as potential targets for drug treatment of the irritable bowel syndrome. Br. J. Pharmacol. 141, 1294-1302 (2004).
62. Finger, T. E. et al. ATP signaling is crucial for communication from taste buds to gustatory nerves. Science 310, 1495-1499 (2005).
63. Gourine, A. V. On the peripheral and central chemoreception and control of breathing: an emerging role of ATP. J. Physiol. (Lond.) 568, 715-724 (2005).
64. Gourine, A. V., Llaudet, E., Dale, N. & Spyer, K. M. ATP is a mediator of chemosensory transduction in the central nervous system. Nature 436, 108-111 (2005).
65. Cockcroft, S. & Gomperts, B. D. ATP induces nucleotide permeability in rat mast cells. Nature 279, 541-542 (1979).
66. Gordon, J. L. Extracellular ATP: effects, sources and fate. Biochem. J. 233, 309-319 (1986).
67. 7). Science 272, 735-738 (1996).
68. 7 receptors. J. Biol. Chem. 276, 125-132 (2001).
69. 7 receptor alters leukocyte function and attenuates an inflammatory response. J. Immunol. 168, 6436-6445 (2002).
70. 7 nucleotide receptor reveals its regulatory roles in bone formation and resorption. Mol. Endocrinol. 17, 1356-1367 (2003).
71. Virginio, C., MacKenzie, A., Rassendren, F. A., North, R. A. & Surprenant, A. Pore dilation of neuronal P2X receptor channels. Nature Neurosci. 2, 315-321 (1999).
72. 7 receptors. Am. J. Physiol. Cell Physiol. 289, C1295-C1302 (2005).
73. Elliott, J. I. et al. Membrane phosphatidylserine distribution as a non-apoptotic signalling mechanism in lymphocytes. Nature Cell Biol. 7, 808-816 (2005).
74. 7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 114, 386-396 (2005).
75. Ma, W. et al. Pore properties and pharmacological features of the P2X receptor channel in airway ciliated cells. J. Physiol. (Lond.) 571, 503-517 (2006).
76. 4-deficient mice. Nature Med. 12, 133-137 (2006).
77. Agboh, K. C., Webb, T. E., Evans, R. J. & Ennion, S. J. Functional characterization of a P2X receptor from Schistosoma mansoni. J. Biol. Chem. 279, 41650-41657 (2004).